Adaptation to Partial Resistance to Powdery Mildew in the Hop Cultivar Cascade by Podosphaera macularis

Abstract

The hop cultivar Cascade has been grown in the Pacific Northwestern U.S. and elsewhere with minimal input for management of powdery mildew (Podosphaera macularis) for nearly 15 years due to the putatively quantitative resistance in this cultivar. While partial resistance is generally thought to be more durable than qualitative resistance, in 2012, powdery mildew was reported on Cascade in Washington State. Field surveys conducted during 2013 to 2016 indicated increasing prevalence of powdery mildew on Cascade, as well as an increasing number of fungicide applications applied to this cultivar in Washington State. Nearly all isolates of P. macularis tested were able to infect Cascade in laboratory inoculations. However, the greatest number of colonies, most conidia produced, and the shortest latent period was only observed with isolates derived originally from Cascade, as compared with other isolates derived from other cultivars. Further, the enhanced aggressiveness of these isolates was only manifested on Cascade and not six other susceptible cultivars, further indicating a specific adaptation to Cascade by the isolates. There was no evidence of a known major R-gene in Cascade, as seven isolates of P. macularis with contrasting virulence all infected Cascade. Among 158 isolates obtained from hop yards planted to Cascade, only two (1.3%) were able to infect the cultivar Nugget, which possesses the resistance factor termed R6, indicating that isolates of P. macularis virulent on Nugget are largely distinct from those adapted to Cascade. Further, race characterization indicated Cascade-adapted isolates of P. macularis were able to overcome R-genes Rb, R3, and R5, but not other known R-genes. Therefore, multiple R-genes and other sources of partial resistance are expected to provide resistance to Cascade-adapted strains of the fungus. Given the plasticity of the powdery mildew fungus, breeding strategies for powdery mildew need to consider the potential for adaptation to both qualitative and partial resistance in the host.

A draft phased assembly of the diploid Cascade hop (Humulus lupulus) genome

“…Powdery mildew reduces the quality and quantity of yield while increasing the cost of production (Henning et al., 2017a). Although Cascade has possessed disease resistance to fungal pathogens powdery mildew ( Podosphaera macularis ) (Gent et al., 2017) and downy mildew ( Pseudoperonospora humuli ) (Henning et al., 2015), these fungal pathogens have the potential to evolve and acquire resistance. A recent outbreak of powdery mildew affecting Cascade in the U.S. Pacific Northwest (PNW) was the result of a Cascade‐adapted isolate of P. macularis (Gent et al., 2017).…”

A phased, diploid assembly of the Cascade hop (Humulus lupulus) genome reveals patterns of selection and haplotype variation

“…Modern research has revealed numerous compounds of medicinal interest in hop with activity against metabolic syndrome [7–9], and with anti-cancer [2, 10, 11], anti-microbial [2, 8, 12], and phytoestrogenic [13–16] properties. Cascade is a backcross hybrid of English and Russian varieties of hop [17] and is the most widely used hop cultivar in craft brewing [18].…”

“…Powdery mildew reduces the quality and quantity of yield while increasing the cost of production [26]. Although Cascade has historically possessed disease resistance to fungal pathogens powdery mildew (Podosphaero macularis) [18] and downy mildew (Pseudoperonospora humuli) [27], there are still risks of damage by these fungal pathogens. A recent outbreak of powdery mildew affecting Cascade in the U.S. Pacific Northwest (PNW) was the result of a Cascade-adapted isolate of P. Macularis [18].…”

“…Although Cascade has historically possessed disease resistance to fungal pathogens powdery mildew (Podosphaero macularis) [18] and downy mildew (Pseudoperonospora humuli) [27], there are still risks of damage by these fungal pathogens. A recent outbreak of powdery mildew affecting Cascade in the U.S. Pacific Northwest (PNW) was the result of a Cascade-adapted isolate of P. Macularis [18]. Very little management was required to grow Cascade until powdery mildew was introduced in the PNW in the mid-1990s [28], and the rise of PM infection corresponds to an increase in Cascade acreage [18].…”

“…A recent outbreak of powdery mildew affecting Cascade in the U.S. Pacific Northwest (PNW) was the result of a Cascade-adapted isolate of P. Macularis [18]. Very little management was required to grow Cascade until powdery mildew was introduced in the PNW in the mid-1990s [28], and the rise of PM infection corresponds to an increase in Cascade acreage [18]. Hop breeding with resistant cultivars [26, 27, 29] can result in new resistance, but given the inevitability of pathogen adaptation, an understanding of the genomic features underlying resistance and susceptibility is necessary to breed for hop that can withstand pathogen adaptations.…”